Statistical mechanics for real biological networks
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1 Statistical mechanics for real biological networks William Bialek Joseph Henry Laboratories of Physics, and Lewis-Sigler Institute for Integrative Genomics Princeton University Initiative for the Theoretical Sciences The Graduate Center City University of New York Colloquium, Santa Fe Institute Thursday, 27 October, 2011
2 Many of the phenomena of life emerge from interactions among large numbers of simpler elements: A network how do we state of one state of the which states get from element in whole are sampled one state to the network network in real life? the next? (from R Segev & a percept, memory, motor plan or thought expression level of one gene fate of a cell during embryonic development choice of amino acid at one site in a protein sequence: structure & function flight direction and speed of one bird in a flock coherent migration coding capacity, multiple attractors,...? ion channels and synapses diffusion, binding, walking,... how many fates? modules vs. emergence? evolution how large is the repertoire? A σ30 LPEGWEMRFTVDGIPYFVDHNRRTTTYIDP ----WETRIDPHGRPYYVDHTTRTTTWERP LPPGWERRVDPRGRVYYVDHNTRTTTWQRP LPPGWEKREQ-NGRVYFVNHNTRTTQWEDP LPLGWEKRVDNRGRFYYVDHNTRTTTWQRP LPNGWEKRQD-NGRVYYVNHNTRTTQWEDP LPPGWEMKYTSEGIRYFVDHNKRATTFKDP LPPGWEQRVDQHGRAYYVDHVEKRTT---LPPGWERRVDNMGRIYYVDHFTRTTTWQRP... B Mutual information (bits) propagation of information, responsiveness,...? sensorimotor response + Newton residue position spike/silence from one neuron σn {σn } P ({σn }) {σn }t {σn }t+ t residue position
3 There is a long history of physicists trying to use ideas from statistical mechanics to approach these systems... approximate dynamics Lyapunov function energy landscape on space of states stable states (stored memories, answers to computations,...) are energy minima If there is a statistical mechanics of network states, there is a phase diagram as networks get large... Where are we in this space? On a critical surface, perhaps? But how do we connect these ideas to real data?
4 Once again, what did we want to know about the system? How do we get from one state to another? Which states of the whole system are sampled in real life? {σ n } t {σ n } t+ t P ({σ n }) State space is too large to answer these (and other) questions directly by experiment. You can t measure all the states, but you can measure averages, correlations,.... Could we build the minimally structured model that is consistent with these measurements? Minimally structured = maximum entropy, and this connects the real data directly to statistical mechanics ideas (!).
5 Network information and connected correlations. E Schneidman, S Still, MJ Berry II & W Bialek, Phys Rev Lett 91, (2003); arxiv:physics/ (2003). Weak pairwise correlations imply strongly correlated network states in a neural population. E Schneidman, MJ Berry II, R Segev & W Bialek, Nature 440, (2006); arxiv:q-bio.nc/ (2005). Ising models for networks of real neurons. G Tkacik, E Schneidman, MJ Berry II & W Bialek, arxiv:q-bio.nc/ (2006). Rediscovering the power of pairwise interactions. W Bialek & R Ranganathan, arxiv: (2007). Statistical mechanics of letters in words. GJ Stephens & W Bialek, Phys Rev E 81, (2010); arxiv:0801,0253 [q-bio.nc] (2008). Spin glass models for networks of real neurons. G Tkacik, E Schneidman, MJ Berry II & W Bialek, arxiv: [q-bio.nc] (2009). Maximum entropy models for antibody diversity. T Mora, AM Walczak, W Bialek & CG Callan, Jr, Proc Nat l Acad Sci (USA) 107, (2010); arxiv: (2009). Are biological systems poised at criticality? T Mora & W Bialek, J Stat Phys 144, (2011); arxiv: [q-bio.qm] (2010). When are correlations strong? F Azhar & W Bialek, arxiv: [q-bio.nc] (2010). Statistical mechanics for a natural flock of birds W Bialek, A Cavagna, I Giardina, T Mora, E Silverstri, M Viale & AM Walczak, arxiv: [physics.bio-ph] (2011). and, most importantly, work in progress.
6 1. Basics of maximum entropy construction 2. The case of neurons in the retina 3. A bit about proteins, birds, Perspective (a few words about the retinal experiments) D Amodei, O Marre & MJ Berry II, in preparation (2011).
7 Let s define various function of the state of the system, f 1 ({σ n }),f 2 ({σ n }),,f K ({σ n }), and assume that experiments can tell us the averages of these functions: f 1 ({σ n }), f 2 ({σ n }),, f K ({σ n }). What is the least structured distribution P ({σ n }) that can reproduce these measured averages? P ({σ n })= 1 Z({g µ }) exp [ K µ=1 g µ f µ ({σ n }) Still must adjust the coupling constants {g µ } ] This tells us the form of the distribution. Matching expectation values = maximum likelihood inference of parameters. to match the measured expectation values.
8 Reminder: Suppose this is a physical system, and there is some energy for each state, E({σ n }) Thermal equilibrium is described by a distribution that is as random as possible (maximum entropy) while reproducing the observed average energy: P ({σ n })= 1 Z exp [ βe({σ n})]] In this view, the temperature T =1/(k B β) is just a parameter we adjust to reproduce E({σ n }).
9 We can think of the maximum entropy construction as defining an effective energy for every state, E({σ n })= K µ=1 g µ f µ ({σ n }), with k B T =1. This is an exact mapping, not an analogy. Examples for neurons: { f µ } = probability of spike vs. silence E = n h n σ n spike probability + pairwise correlations probability that M cells spike together E = h n σ n n ( E = V n σ n ) nm J nm σ n σ m this case we can do analytically
10 maximum entropy model consistent with probability of M cells spiking together E = V ( n σ n ) Find this global potential for multiple subgroups of N neurons. Lots of states with the same energy... count them to get the entropy. For large N we expect entropy and energy both proportional to N. Plot of S/N vs. E/N contains all the thermodynamics of the system. entropy per neuron What we see is (within errors) S = E. This is very weird. N= extrapolation S = (0.985 ± 0.008)E energy per neuron
11 The real problem: maximum entropy model consistent with mean spike probabilities, pairwise correlations, and probabilities of M cells spiking together. E = n h n σ n nm J nm σ n σ m + V There are lots of parameters, but we can find them all from ~1 hour of data. This is a hard inverse statistical mechanics problem. ( n σ n ) one example of 100 neurons Correlations reproduced within error bars. ln[p(data)] No sign of over-fitting. training segments test segments
12 For small networks, we can test the model by checking the probability of every state. For larger networks, we can check connected higher order (e.g. 3-cell) correlations. (example w/n=10) N=100, matching pairwise correlations N=100, matching pairwise + P(M) matching pairwise correlations matching pairwise + P(M) mean absolute error of predicted 3-cell correlations Seems to be working even better for larger N.
13 Where are we in parameter space? One direction in parameter space corresponds to changing temperature... let s try this one: specific heat (per neuron) N= The system is poised very close to a point in parameter space where the specific heat is maximized - a critical point. heat capacity independent Can we do experiments to show that the system adapts to hold itself at criticality? temperature specific heat = variance of energy = variance of log(probability) Having this be large is exactly the opposite of the usual criteria for efficient coding (!). Instead, does operation near the critical point maximize the dynamic range for representing surprise?
14 Can use the same strategy to make models for... the distribution of amino acids in a family of proteins, A σ 30 LPEGWEMRFTVDGIPYFVDHNRRTTTYIDP ----WETRIDPHGRPYYVDHTTRTTTWERP LPPGWERRVDPRGRVYYVDHNTRTTTWQRP LPPGWEKREQ-NGRVYFVNHNTRTTQWEDP LPLGWEKRVDNRGRFYYVDHNTRTTTWQRP LPNGWEKRQD-NGRVYYVNHNTRTTQWEDP LPPGWEMKYTSEGIRYFVDHNKRATTFKDP LPPGWEQRVDQHGRAYYVDHVEKRTT---- LPPGWERRVDNMGRIYYVDHFTRTTTWQRP... or the flight velocities of birds in a flock. B Mutual information (bits) 1 residue position residue position
15 Observed Model Independent Probability Rank For protein families (here, antibodies), look at the Zipf plot. This is S vs. E, turned on its side; unit slope implies S = E (again!). For birds, look at the correlations directly in real space (as usual in stat mech). ALL of these, as with the specific heat in our neural network, are signatures that the real system is operating near a critical point in its parameter space.
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